Abstract
Balancing growth and stress tolerance helps plants survive unfavorable environments such as hypoxia caused by submergence. However, the underlying mechanisms by which plant cells fine-tune growth and responses to hypoxia remain unclear. Here, we identified an Arabidopsis (Arabidopsis thaliana) RELATED TO APETALA2 (RAP2) transcription factor, RAP2.4h, that functions in controlling the energy-signaling-mediated trade-off between growth and tolerance of hypoxia. The Arabidopsis RAP2.4h knockout mutant showed increased tolerance of hypoxia and reduced vegetative growth; transgenic lines overexpressing RAP2.4h (RAP2.4h-OE) showed decreased tolerance of hypoxia with increased vegetative growth. During hypoxia, the α-catalytic KIN10 subunit of the energy sensor SnRK1 interacted with and phosphorylated RAP2.4h, thereby suppressing RAP2.4h transcription. Under normoxic conditions, RAP2.4h directly targeted the promoters of the aquaporin genes PIP2;1 and PIP2;2, stimulating their expression. Loss of PIP2;1 and PIP2;2 function rescued the hypoxia hypersensitivity and excessive vegetative growth of RAP2.4h-OE lines. Analyzing the hypoxia sensitivity and growth phenotypes of OsRAP2.4h-knockout mutants in rice (Oryza sativa) revealed functional conservation of the RAP2.4h–PIP2 module in rice and Arabidopsis. Thus, this work uncovers a genetic link connecting energy signaling with the hypoxia response and demonstrates that the SnRK1–RAP2.4h–PIP2 module functions to balance growth and hypoxia tolerance in plants.
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Acknowledgements
The authors thank the ABRC (www.arabidopsis.org) for providing rap2.4h mutant seeds, Prof. Qi Xie (Institute of Genetics and Developmental Biology, Chinese Academy of Sciences) for providing pip2;1 pip2;2 mutant, PIP2;1-OE1, and PIP2;2-OE1 seeds, Prof. Ming-Yi Bai (Shandong University) for providing kin10, kin11, kin10−/− kin11+/−, and kin10+/− kin11−/− mutant seeds, Prof. Chen-Long Li (Sun Yat-sen University) for assistance in ChIP-qPCR and ChIP-seq analyses, and Prof. Hong-Bin Wang (Guangzhou University of Chinese Medicine) for assistance in measurement of photosynthetic capacity.
Funding
This work was supported by the National Natural Science Foundation of China (Projects 32321163646 [S.X.] and U22A20458 [S.X.]) and the Natural Science Foundation of Guangdong Province (Project 2023A1515012038 [Q.F.C.]).
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Liao, K., Wang, LN., Lu, XY. et al. The SnRK1–RAP2.4h–PIP2 module contributes to the trade-off between growth and hypoxia tolerance in plants. Nat Commun (2026). https://doi.org/10.1038/s41467-026-72469-7
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DOI: https://doi.org/10.1038/s41467-026-72469-7
